Integrity of all four transmembrane domains of the tetraspanin uroplakin Ib is required for its exit from the ER

Journal of Cell Science

Volumn 119, Issue 24, 2006, Pages 5077-5086

  Tu, Liyu ^a   Kong, Xiang Peng ^a   Sun, Tung Tien ^a   Kreibich, Gert ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endoplasmic reticulum; Membrane proteins; Tetraspanins; Uroplakins

Indexed keywords

CYSTEINE; DISULFIDE; MEMBRANE PROTEIN; TETRASPANIN; UNCLASSIFIED DRUG; UROPLAKIN; UROPLAKIN IA; UROPLAKIN IB; UROPLAKIN II; UROPLAKIN IIIA;

ARTICLE; CELL SURFACE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EXTRACELLULAR SPACE; GENE MUTATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BLOTTING, WESTERN; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOPLASMIC RETICULUM; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; LUMINESCENT PROTEINS; MEMBRANE GLYCOPROTEINS; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT;

MAMMALIA;

EID: 33846165776     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03285     Document Type: Article

References (54)

1. Barlowe, C. (2003). Signals for COPII-dependent export from the ER: what's the ticket out? Trends Cell Biol. 13, 295-300.
2. Berditchevski, F., Odintsova, E., Sawada, S. and Gilbert, E. (2002). Expression of the palmitoylation-deficient CD151 weakens the association of alpha 3 beta 1 integrin with the tetraspanin-enriched microdomains and affects integrin-dependent, signaling. J. Biol. Chem. 277, 36991-37000.
3. Bonifacino, J. S., Suzuki, C. K. and Klausner, R. D. (1990). A peptide sequence confers retention and rapid degradation in the endoplasmic reticulum. Science 247, 79-82.
4. Bowie, J. U. (1999). Helix-bundle membrane protein fold templates. Protein Sci. 8, 2711-2719.
5. Cannon, K. S. and Cresswell, P. (2001). Quality control of transmembrane domain assembly in the tetraspanin CD82. EMBO J. 20, 2443-2453.
6. Deng, F. M., Liang, F. X., Tu, L., Resing, K. A., Hu, P., Supino, M., Hu, C. C., Zhou, G., Ding, M., Kreibich, G. et al. (2002). Uroplakin IIIb, a urothelial differentiation marker. dimerizes with uroplakin Ib as an early step of urothelial plaque assembly. J. Cell Biol. 159, 685-694.
7. Dominguez, M., Dejgaard, K., Fullekrug, J., Dahan, S., Fazel, A., Paccaud, J. P., Thomas, D. Y., Bergeron, J. J. and Nilsson, T. (1998). gp25L/emp24/p24 protein family members of the cis-Golgi network bind both COP I and II coatomer. J. Cell Biol. 140, 751-765.
8. Dutzler, R., Campbell, E. B., Cadene, M., Chait, B. T. and MacKinnon, R. (2002). X-ray structure of a CIC chloride channel at 3.0 A reveals the molecular basis of anion selectivity. Nature 415, 287-294.
9. Ellgaard, L. and Helenius, A. (2003). Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4, 181-191.
10. Fu, J. and Kreibich, G. (2000). Retention of subunits of the oligosaccharyltransferase Complex in the endoplasmic reticulum. J. Biol. Chem. 275. 3984-3990.
11. Fu, J., Pirozzi, G., Sanjay, A., Levy, R., Chen, Y., De Lemos-Chiarandini, C., Sabatini, D. and Kreibich, G. (2000). Localization of ribophorin II to the endoplasmic reticulum involves both its transmembrane and cytoplasmic domains. Eur J. Cell Biol. 79, 219-228.
12. Garcia-Espana, A., Chung, P. J., Zhao, X., Lee, A., Pellicer, A., Yu, J., Sun, T. T. and Desalle, R. (2006). Origin of the tetraspanin uroplakins and their co-evolution with associated proteins: implications for uroplakin structure and function. Mol. Phylogenet. Evol. 41, 355-367.
13. Gratkowski, H., Lear, J. D. and DeGrado, W. F. (2001). Polar side chains drive the association of model transmembrane peptides. Proc. Natl. Acad. Sci. USA 98, 880-885,
14. Hammond, C., Braakman, I. and Helenius, A. (1994). Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc. Natl. Acad. Sci. USA 91, 913-917.
15. Hemler, M. E. (2001). Specific tetraspanin functions. J. Cell Biol. 155, 1103-1107.
16. Hemler, M. E. (2003). Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu. Rev. Cell Dev. Biol. 19, 397-422.
17. Hessa, T., Kim, H., Bihlmaier, K., Lundin, C., Boekel, J., Andersson, H., Nilsson, I., White, S. H. and von Heijne, G. (2005). Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433, 377-381.
18. Hicks, R. M. ( 1965). The fine structure of the transitional epithelium of Rat ureter. J Cell Biol. 26, 25-48.
19. Hu, P., Deng, F. M., Liang, F. X., Hu, C. M., Auerbach, A. B., Shapiro, E., Wu, X. R., Kachar, B. and Sun, T. T. (2000). Ablation of uroplakin III gene results in small urothelial plaques, urothelial leakage, and vesicoureteral reflux. J Cell Biol. 151, 961-972.
20. Kachar, B., Liang, F., Lins, U., Ding, M., Wu, X. R., Stoffler, D., Aebi, U. and Sun, T. T. (1999). Three-dimensional analysis of the 16 nm urothelial plaque particle: luminal surface exposure, preferential head-to-head interaction, and hinge formation. J. Mol Biol. 285, 595-608.
21. Kelleher, D. J., Kreibich, G. and Gilmore, R. (1992). Oligosaccharyltransferase activity is associated with a protein complex composed of ribophorins I and II and a 48 kd protein. Cell 69, 55-65.
22. Klausner, R. D., Lippincott-Schwartz, J. and Bonifacino, J. S. (1990). The T cell antigen receptor: insights into organelle biology. Annu. Rev. Cell Biol. 6, 403-431.
23. Kong, X. T., Deng, F. M., Hu, P., Liang, F. X., Zhou, G., Auerbach, A. B., Genieser, N., Nelson, P. K., Robbins, E. S., Shapiro, E. et al. (2004). Roles of uroplakins in plaque formation, umbrella cell enlargement, and urinary tract diseases. J. Cell Biol. 167, 1195-1204.
24. Kota, J. and Ljungdahl, P. O. (2005). Specialized membrane-localized chaperones prevent aggregation of polytopic proteins in the ER. J. Cell Biol. 168, 79-88.
25. Kovalenko, O. V., Metcalf, D. G., Degrado, W. F. and Hemler, M. E. (2005). Structural organization and interactions of transmembrane domains in tetraspanin proteins. BMC Struct. Biol. 5, 11.
26. Krebs, M. R., Macphee, C. E., Miller, A. F., Dunlop, I. E., Dobson, C. M. and Donald, A. M. (2004). The formation of spherulites by amyloid fibrils of bovine insulin. Proc. Natl. Acad. Sci. USA 101, 14420-14424.
27. Langosch, D. and Heringa, J. (1998). Interaction of transmembrane helices by a knobs-into-holes packing characteristic of soluble coiled coils. Proteins 31, 150-159.
28. Letourneur, F. and Klausner, R. D. (1992). A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 69, 1143-1157.
29. Liang, F. X., Riedel, I., Deng, F. M., Zhou, G., Xu, C., Wu, X. R., Kong, X. P., Moll, R. and Sun, T. T. (2001). Organization of uroplakin subunits: transmembrane topology, pair formation and plaque composition. Biochem. J. 355, 13-18.
30. Lin, J. H., Wu, X. R., Kreibich, G. and Sun, T. T. (1994). Precursor sequence, processing, and urothelium-specific expression of a major 15-kDa protein subunit of asymmetric unit membrane. J. Biol. Chem. 269, 1775-1784.
31. Min, G., Zhou, G., Schapira, M., Sun, T. T. and Kong, X. P. (2003). Structural basis of urothelial permeability barrier function as revealed by Cryo-EM studies of the 16 nm uroplakin particle. J. Cell Sci. 116, 4087-4094.
32. Min, G., Wang, H., Sun, T. T. and Kong, X. P. (2006). Structural basis for tetraspanin functions as revealed by the cryo-EM structure of uroplakin complexes at 6-A resolution. J. Cell Biol. 173, 975-983.
33. Nikonov, A. V., Snapp, E., Lippincott-Schwartz, J. and Kreibich, G. (2002). Active translocon complexes labeled with GFP-Dad1 diffuse slowly as large polysome arrays in the endoplasmic reticulum. J. Cell Biol. 158, 497-506.
34. Otte, S. and Barlowe, C. (2002). The Erv41p-Erv46p complex: multiple export signals are required in trans for COPII-dependent transport from the ER. EMBO J. 21, 6095-6104.
35. Porter, K. R., Kenyon, K. and Badenhausen, S. (1967). Specializations of the unit membrane. Protoplasma 63, 263-274.
36. Schamel, W. W., Kuppig, S., Becker, B., Gimborn, K., Hauri, H. P. and Reth, M. (2003). A high-molecular-weight complex of membrane proteins BAP29/BAP31 is involved in the retention of membrane-bound IgD in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 100, 9861-9866.
37. Schneider, D. (2004). Rendezvous in a membrane: close packing, hydrogen bonding, and the formation of transmembrane helix oligomers. FEBS Lett. 577, 5-8.
38. Seigneuret, M. (2006). Complete predicted three-dimensional structure of the facilitator transmembrane protein and hepatitis C virus receptor CD81: conserved and variable structural domains in the tetraspanin superfamily. Biophys. J. 90, 212-227.
39. Seigneuret, M., Delaguillaumie, A., Lagaudriere-Gesbert, C. and Conjeaud, H. (2001). Structure of the tetraspanin main extracellular domain. A partially conserved fold with a structurally variable domain insertion. J. Biol. Chem. 276, 40055-40064.
40. Sekijima, Y., Wiseman, R. L., Matteson, J., Hammarstrom, P., Miller, S. R., Sawkar, A. R., Balch, W. E. and Kelly, J. W. (2005). The biological and chemical basis for tissue-selective amyloid disease. Cell 121, 73-85.
41. Sevier, C. S., Weisz, O. A., Davis, M. and Machamer, C. E. (2000). Efficient export of the vesicular stomatitis virus G protein from the endoplasmic reticulum requires a signal in the cytoplasmic tail that includes both tyrosine-based and di-acidic motifs. Mol. Biol. Cell 11, 13-22.
42. Staehelin, L. A., Chlapowski, F. J. and Bonnevile, M. A. (1972). Lumenal plasma membrane of the urinary bladder. I. Three-dimentional reconstruction from freeze-etch images. J. Cell Biol. 53, 73-91.
43. Stipp, C. S., Kolesnikova, T. V. and Hemler, M. E. (2003). Functional domains in tetraspanin proteins. Trends Biochem. Sci. 28, 106-112.
44. Swanton, E., High, S. and Woodman, P. (2003). Role of calnexin in the glycan-independent quality control of proteolipid protein. EMBO J. 22, 2948-2958.
45. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting. position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
46. Tu L., Sun, T. T. and Kreibich, G. (2002). Specific heterodimer formation is a prerequisite for uroplakins to exit from the endoplasmic reticulum. Mol. Biol. Cell 13, 4221-4230.
47. Ward, T. H., Polishchuk, R. S., Caplan, S., Hirschberg, K. and Lippincott-Schwartz, J. (2001). Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol. 155, 557-570.
48. White, S. H. (2003). Translocons, thermodynamics, and the folding of membrane proteins. FEBS Lett. 555, 116-121.
49. Wu, X. R. and Sun, T. T. (1993). Molecular cloning of a 47 kDa tissue-specific and differentiation-dependent urothelial cell surface glycoprotein. J. Cell Sci. 106, 31-43.
50. Wu, X. R., Manabe, M., Yu, J. and Sun, T. T. (1990). Large scale purification and immunolocalization of bovine uroplakins I, II, and III. Molecular markers of urothelial differentiation. J. Biol. Chem. 265, 19170-19179.
51. Wu, X. R., Lin, J. H., Walz, T., Haner, M., Yu, J., Aebi, U. and Sun, T. T. (1994). Mammalian uroplakins. A group of highly conserved urothetial differentiation-related membrane proteins. J. Biol. Chem. 269, 13716-13724.
52. Wu, X. R., Medina, J. J. and Sun, T. T. (1995). Selective interactions of UPIa and UPIb, two members of' the transmembrane 4 superfamily, with distinct single transmembrane-domained proteins in differentiated urothelial cells. J. Biol. Chem. 270, 29752-29759.
53. Yu, J., Lin, J. H., Wu, X. R. and Sun, T. T. (1994). Uroplakins Ia and Ib, two major differentiation products of bladder epithelium, belong to a family of four transmembrane domain (4TM) proteins. J Cell Biol. 125, 171-182.
54. Zhou, F. X., Cocco, M. J., Russ, W. P., Brunger, A. T. and Engelman, D. M. (2000). Interhelical hydrogen bonding drives strong interactions in membrane proteins. Nat. Struct. Biol. 7, 154-160.